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356 



Journal of the American Mosquito Control Association 



Vol. 4, No. 3 



AEDES ALBOPICTUS IN THE UNITED STATES: RAPID SPREAD OF A 
POTENTIAL DISEASE VECTOR 

C. G. MOORE, D. B. FRANCY, D. A. ELIASON and T. P. MONATH 

Division of Vector-Borne Viral Diseases, Center for Infectious Diseases, Centers for Disease Control, Public 
Health Service, U. S. Department of Health and Human Services, P. 0. Box 2087, Fort Collins, CO 80522 

ABSTRACT. Aedes albopictus, the Asian "tiger mosquito," was found in Houston, Texas, in 1985. 
Aedes albopictus is primarily a forest edge inhabiting species that has readily adapted to the container 
habitats produced by humans. Although not yet incriminated in the spread of any disease in the 
Americas, it has been repeatedly implicated in epidemic dengue and dengue hemorrhagic fever transmis- 
sion in Asia. It is a competent laboratory vector of La Crosse, yellow fever and other viruses, and can 
transovarially transmit at least 15 viruses. In 1986, Ae. albopictus was found in many other Texas 
counties, and in Alabama, Arkansas, Florida, Georgia, Illinois, Indiana, Louisiana, Mississippi, Missouri, 
Ohio, and Tennessee. In 1987, infestations were discovered in Delaware, Kentucky, Maryland, and North 
Carolina. Aedes albopictus and other exotic species were intercepted in shipments of used tires entering 
the United States from Asia. All such tires must now be free of mosquitoes before entering the country. 
Control over the movement and storage of tires, a strong source reduction program, and intensive public 
education can solve the albopictus problem. 



INTRODUCTION 

On August 2, 1985, the Harris County Mos- 
quito Control District in Houston, Texas, dis- 
covered that Aedes albopictus (Skuse), a mos- 
quito of Asian origin, was established in Harris 
County (Sprenger and Wuithiranyagool 1986). 
The identification was confirmed by the U. S. 
National Museum, and the Centers for Disease 
Control (CDC) was notified of the infestation 
on January 31, 1986. The CDC in turn notified 
the appropriate state, federal, and international 
agencies. Although Ae. albopictus had been col- 
lected previously in the United States (Reiter 
and Darsie 1984), this was the first report of 
breeding populations established in this hemi- 
sphere. 

This species, commonly known as the "Asian 
tiger mosquito" (Robertson and Hu 1935), is 
found from Madagascar eastward through Asia 
to Japan, Korea, and northern China (Knight 
and Stone 1977, Huang 1972). It is also present 
in Hawaii. 

In Asia, Ae. albopictus is primarily a forest 
edge inhabiting species (Lu et al. 1980), giving 
way to other Aedes species inside forested areas. 
It has readily adapted to the container habitats 
produced by humans. Aedes albopictus is not as 
strongly dependent on humans as Ae. aegypti 
(Linn.); it could colonize tree holes and other 
similar habitats in the eastern United States, 
making control extremely difficult. 

Field and laboratory studies of competition 
between tropical Asian strains of Ae. albopictus 
and Ae. aegypti suggested that aegypti would 
eliminate albopictus (Gilotra et al. 1967, Moore 
and Fisher 1969). In Hawaii, however, the re- 
verse happened (Usinger 1944), possibly because 
aegypti is near the limit of its northern distri- 
bution. Recent studies by Hawley et al. (1986) 



indicate the U. S. strains of albopictus are of 
northern Asian origin, and these strains may be 
better adapted than aegypti to the more temper- 
ate ecological conditions of the United States 
(Nawrocki and Hawley 1987). Moreover, work- 
ers in several states observe that albopictus is 
replacing aegypti. 

Aedes albopictus has been repeatedly impli- 
cated in epidemic dengue and dengue hemor- 
rhagic fever transmission in Asia (Metselaar et 
al. 1980, Jumali et al. 1979). Laboratory studies 
also have confirmed its efficiency as a dengue 
vector (Boromisa et al. 1987, Mitchell et al. 
1987). This species is a competent vector of 
California encephalitis group viruses (Shroyer 
1986a, P. R. Grimstad et al., unpublished data), 
yellow fever and epidemic polyarthritis (Ross 
River) viruses (Mitchell and Gubler 1987, 
Mitchell et al. 1987), and other agents (Shroyer 
1986b). In addition, Ae. albopictus can transmit 
transovarially at least 15 viruses (Shroyer 
1986b); it is not an effective vector of St. Louis 
or Venezuelan equine encephalitis viruses (D. B. 
Francy, unpublished data). 

Aedes albopictus has not yet been incriminated 
in the spread of any disease in the Americas, 
and probably will not be until the level of mos- 
quito-reservoir and human-mosquito contact ex- 
ceeds some threshold; the potential impact of a 
vector such as Ae. albopictus in a new environ- 
ment is difficult to predict. Although dengue 
epidemics have occurred principally in the Gulf 
Coast states, where Ae. aegypti already occurs, a 
major Ae. aegypta'-transmitted dengue epidemic 
occurred in Philadelphia in the late 18th century 
(Wisseman and Sweet 1961, Anonymous 1977). 
The presence of a new, competent vector in the 
northern United States could mean a resurgence 
of dengue in those areas. Of more immediate 
concern is the presence of Ae. albopictus in La 



September 1988 



Spread of Ae. albopictus in the United States 



357 



Crosse-endemic portions of the eastern United 
States. Since that virus is already present, the 
possibility of a vectorial role seems higher than 
for other viruses. The ability of Ae. albopictus to 
transmit yellow fever is of concern because the 
species was introduced into Brazil in 1986 (Cen- 
ters for Disease Control 1986b). This mosquito 
can breed in areas removed from human habi- 
tation and might serve as a link between jungle 
and urban cycles of yellow fever. 

We describe here the progressive movement 
of Ae. albopictus in the United States in 1986 
and 1987, as recorded by the Division of Vector- 
Borne Viral Diseases (DVBVD), Centers for 
Disease Control (CDC). State and local health 
department and mosquito control agency per- 
sonnel collaborated in this effort (CDC 1986a, 
1986b, 1986c, 1987). 

DISTRIBUTION AND SPREAD, 
1986-1987 

In their initial survey in Houston, August 
through October 1985, Sprenger and Wuithir- 
anyagool (1986) found that Ae. albopictus was 
widespread, especially in the eastern half of 
Harris county. They found the species in 73.9% 
of water- filled containers with mosquito larvae. 
In 1986, with the advent of warm weather and 
spring rainfall, efforts were begun to determine 
the extent of the infestation in Texas and sur- 
rounding states. During April and May, Ae. al- 
bopictus was found in counties adjacent to Hous- 
ton; in New Orleans, Louisiana, and surround- 
ing parishes; and in Memphis, Tennessee. In 
June and early July, the mosquito was reported 
from Gulfport, Mississippi, and Jacksonville, 
Florida. 

Since 1981, CDC had maintained a collabo- 
rative Aedes aegypti surveillance program, using 
the CDC ovitrap (Fay and Eliason 1966). In 



early 1986, the program was modified and ex- 
panded to better detect Ae. albopictus. The pro- 
gram involved 39 cities (Table 1), of which 10 
were infested with Ae. albopictus. The species 
was found in San Antonio, Texas, as a result of 
the ovitrap program. In 1987, the program was 
expanded to include 59 cities, of which 19 were 
infested (Table 2). Again, one infested city was 
found (in the absence of other surveillance) in 
1987 as a result of the program. 
A systematic survey of 41 cities and towns in 

6 southern states was conducted in July 1986 
(CDC 1986b). Because Ae. albopictus tends to 
oviposit in discarded tires containing rainwater, 
used-tire dumps and premises of tire dealers and 
retreaders were surveyed. Aedes albopictus was 
found to be widely disseminated in the southern 
United States but to have a spotty and discon- 
tinuous distribution (Table 3, Fig. 1A). In many 
sites, Ae. albopictus was abundant and bit hu- 
mans aggressively. The presence of Ae. aegypti 
in an area did not appear to retard the ingress 
of Ae. albopictus, which had replaced the former 
in many locations. 

From September 15-29, 1986, surveys were 
conducted in Ohio, Indiana, Illinois, Missouri, 
Kentucky, and Arkansas. Again mainly the busi- 
ness premises of tire dealers and retreaders were 
inspected. Ae. albopictus was found in at least 1 
location in 2 of 10 counties surveyed in Illinois, 
2 of 16 in Indiana, 3 of 11 in Missouri, and 1 of 

7 in Arkansas; none were found in the Kentucky 
survey. In early September, a single infested site 
had been discovered by the Ohio Department of 
Health in Darke County; no further infestations 
were found during surveys in 5 other Ohio coun- 
ties. Infestations in the northern states were less 
common (13% of 53 counties) than in the heav- 
ily-infested states of Texas, Louisiana, and Mis- 
sissippi (89% of 35 counties surveyed). 

Statewide surveys in 1987 were conducted pri- 



Table 1. Collaborative ovitrap program for Aedes albopictus in the eastern United States, 1986. 





No. 
cities 


Total traps 






Positive ovitraps 








aegypti 


albopictus 

N % 


triseriatus 


State 


N 


% 


N 


% 


Alabama 


5 


375 


68 


18.1 


18 


4.8 


3 


0.8 


Arkansas 


2 


279 


86 


30.8 





0.0 


4 


1.4 


Florida 


8 


1,107 


128 


11.6 


4 


0.04 





0.0 


Georgia 


3 


393 


144 


36.6 





0.0 


35 


8.9 


Kentucky 


1 


36 





0.0 





0.0 





0.0 


Louisiana 


5 


684 


58 


8.5 


19 


2.8 


20 


2.9 


Mississippi 


2 


5 


4 


80.0 


3 


60.0 


1 


20.0 


Missouri 


1 


14 





0.0 


1 


7.0 





0.0 


N. Carolina 


4 


267 


26 


9.7 





0.0 


18 


48.1 


S. Carolina 


4 


354 


108 


30.5 





0.0 


21 


5.9 


Tennessee 


1 


117 


23 


19.7 


51 


43.6 


1 


0.9 


Texas 


3 


233 


60 


25.8 


10 


5.2 


2 


1.0 


Total 


39 


3,864 


705 


18.2 


106 


2.7 


105 


2.7 



358 



Journal of the American Mosquito Control Association Vol. 4 No. 3 



Table 2. Collaborative ovitrap program for Aedes albopictus in 


the eastern United States, 


1987. 




No. 
cities 

8 


Total traps 

1,776 






Positive 


ovitraps 








aegypti 


albopictus 

N % 


triseriatus 


State 


N 


% 


N 


% 


Alabama 


549 


30.9 


147 


8.3 


124 


7.0 


Arkansas 


3 


596 


163 


27.3 


4 


0.7 


5 


0.9 


Florida 


7 


2,794 


357 


12.8 


2 


0.1 





0.0 


Georgia 


3 


873 


162 


18.6 





0.0 


3 


0.3 


Kentucky 


1 


126 





0.0 





0.0 


1 


0.8 


Louisiana 


9 


2,877 


437 


15.2 


343 


11.9 


53 


1.8 


Mississippi 


1 


170 


10 


6.0 


32 


19.0 


2 


1.0 


Missouri 


2 


34 





0.0 





0.0 


10 


29.1 


N. Carolina 


5 


1,095 


235 


21.5 


2 


0.2 


27 


2.4 


Oklahoma 


1 


307 





0.0 





0.0 





0.0 


S. Carolina 


5 


1,163 


281 


24.1 





0.0 


13 


1.1 


Tennessee 


1 


287 


46 


16.0 


46 


16.0 


3 


1.1 


Texas 


7 


1,695 


431 


25.4 


267 


15.8 


8 


0.5 


Virginia 


5 


604 


3 


0.5 





0.0 


27 


4.5 


W. Virginia 


1 


287 





0.0 





0.0 


11 


4.0 


Totals 


59 


14,684 


2,673 


18.2 


844 


5.7 


287 


2.0 



marily by state and local agencies. Additional 
infestations of Ae. albopictus were found in Del- 
aware, Kentucky, North Carolina, and Mary- 
land (Table 3, Fig. IB). Several counties that 
were inspected and found negative in 1986 were 
positive for Ae. albopictus in 1987, suggesting 
expansion of the species rather than discovery 
of preexisting foci. 

In July and August 1987, 8 cities known to be 
infested with Ae. albopictus in Texas, Louisiana, 
Florida, Missouri, Tennessee, and Indiana were 
surveyed in detail to determine how far the 
mosquito had spread from the original foci of 
introduction and how it was spreading. The 
results of that study will be reported separately; 
however, there was a notable decrease in the 
dominance of Ae. albopictus (i.e., albopictus as a 
percent of all container-breeding Aedes spp.) 
with increasing distance from Houston, the first 
known infested city in the United States (Table 
4). 

Despite its rapid northward and eastward ex- 
tension, Ae. albopictus has so far failed to move 
into south Texas or south Florida. The mosqui- 
to's current southern limit is between 29° and 
30° north latitude. The photoperiodic response 
that allows this species to enter diapause (Haw- 
ley et al. 1987), making it uniquely adapted to 
the northern temperature environment, may 
also be limiting its southern spread. If this is 
true, the introduction of strains from more 
southerly locations in Asia could result in south- 
ward extension of the species into Mexico and 
Central America. The Brazilian populations of 
Ae. albopictus (CDC 1986b) are apparently un- 
able to enter diapause (G. B. Craig, Jr., personal 
communication), and may therefore be able to 
occupy much of tropical America. 



INTERCEPTION OF USED TIRES 
FROM ASIA 

Aedes albopictus has been collected or inter- 
cepted in the contiguous United States on 3 
previous occasions (Reiter and Darsie 1984), but 
breeding populations were not demonstrated. 
Because of previous interceptions and the ap- 
parent association of the Houston infestation 
with used tires, CDC began a program of in- 
specting used auto and truck tires entering 
U.S. ports from Asia. Of 3.2 million used tires 
imported into the United States in 1985, 2.8 
million came from Asian countries with indige- 
nous Ae. albopictus populations. In 1986, more 
than 22,000 tires were inspected by CDC, state, 
and local personnel. On October 6-7, 1986, for 
example, inspectors checked 2,613 tires in 9 
cargo containers originating in Japan and off- 
loaded in Seattle, Washington. Aedes albopictus 
larvae were found in 11 tires in 2 of the con- 
tainers (CDC 1986c). The positive containers 
were fumigated with methyl bromide to kill lar- 
vae and eggs. The 1986 inspections produced 15 
tires with mosquito larvae of 5 species belonging 
to 4 genera (Craven et al. 1988). 

In 1987, staff of the Alameda County Mos- 
quito Abatement District collected Ae. albopictus 
larvae from large equipment tires shipped from 
Hawaii to an Oakland, California, tire dealer. 
No additional specimens have been collected at 
the Oakland site, suggesting that the species 
failed to become established. 

Because this mosquito can introduce several 
exotic arboviruses into the United States (via 
transovarially infected eggs or larvae) and con- 
tinued importation of populations from other 
areas can expand the genetic variability of ex- 



September 1988 



Spread of Ae. albopictus in the United States 



359 



Table 3. Aedes albopictus-mtested counties reported to CDC by state and local agencies, 1986 and 1987. 



State & County 



1986* 



1987 



State & County 



1986 



1987 



Alabama 






Mississippi 






Colbert 


+ 


? 


Forrest 


+ 


? 


Covington 


7 


+ 


Harrison 


+ 


+ 


Cullman 


+ 


+ 


Hinds 


+ 


+ 


Jefferson 


- 


+ 


Warren 


+ 


? 


Mobile 


- 


+ 


Missouri 






Arkansas 






Clay 


- 


+ 


Grant 


+ 


? 


Jackson 


+ 


+ 


California 






St. Charles 


+ 


+ 


Alameda 


- 


+ 


St. Louis 


+ 


+ 


Delaware 






Washington 


+ 


? 


Kent 


7 


+ 


North Carolina 






Florida 






New Hanover 


7 


+ 


Duval 


+ 


+ 


Rockingham 


? 


+ 


Georgia 






Stokes 


? 


+ 


Chatham 


+ 


+ 


Mecklenburg 


7 


+ 


Clarke 


? 


+ 


Ohio 






Fulton 


+ 


7 


Darke 


± 


± 


Illinois 






Hancock 


- 


± 


Cook 


- 


+ 


Jackson 


- 


± 


Jefferson 


+ 


? 


Tennessee 






St. Clair 


+ 


? 


Shelby 


+ 


+ 


Indiana 






Texas 






Dearborn 


- 


+ 


Anderson 


+ 


+ 


Marion 


+ 


+ 


Angelina 


7 


+ 


Vanderburgh 


+ 


+ 


Bell 


? 


+ 


Kentucky 






Bexar 


+ 


+ 


Fayette 


- 


+ 


Bowie 


+ 


7 


Louisiana 






Brazoria 


+ 


+ 


Caddo 


+ 


+ 


Chambers 


+ 


+ 


Calcasieu 


+ 


+ 


Coryell 


? 


+ 


E. Baton Rouge 


+ 


+ 


Dallas 


+ 


+ 


Iberia 


+ 


+ 


Ellis 


+ 


+ 


Jefferson 


+ 


+ 


Fort Bend 


+ 


+ 


Lafayette 


? 


+ 


Galveston 


+ 


+ 


Orleans 


+ 


+ 


Harris 


+ 


+ 


Ouachita 


- 


+ 


Houston 


7 


+ 


Plaquemines 


+ 


7 


Jefferson 


+ 


+ 


Rapides 


? 


+ 


Liberty 


+ 


+ 


St. Bernard 


+ 


7 


Montgomery 


+ 


+ 


St. Charles 


+ 


+ 


Orange 


? 


+ 


St. Tammany 


+ 


7 


Rusk 


? 


+ 


Tangipahoa 


+ 


? 


San Jacinto 


+ 


+ 


Vermilion 


+ 


+ 


Tarrant 


+ 


+ 


Vernon 


? 


+ 


Tyler 


? 


+ 


Maryland 






Walker 


? 


+ 


Baltimore 


? 


+ 


Webb 


+ 


- 



"+" - positive; "-" = negative; "±" = positive, but population was eradicated or area became negative 
without treatment; "?" = unknown, not surveyed. 



isting populations, additional introductions 
must be prevented. On January 1, 1988, under 
the provisions of Public Law 78-410, Public 
Health Service Act, Section 361, and 42 CFR 
71.32(c)(10), CDC required that all used tire 
casings from Asia be certified as dry, clean, and 
free of insects. The CDC is now monitoring 
compliance with this regulation. 

OPTIONS FOR CONTROL 

Dealing with existing U. S. A. populations of 
Ae. albopictus is more difficult than preventing 



continued introductions from other countries. 
Responses by different state and local agencies 
have varied from no action to attempted eradi- 
cation of foci. Permanent solutions are unlikely 
as long as used tires are moved freely in inter- 
state commerce without some disinsectization 
requirement. One relatively inexpensive way to 
reduce the spread of Ae. albopictus is to require 
that tires be stored and shipped without water. 
Insecticide susceptibility tests by the New 
Orleans Mosquito Control Board, Rutgers Uni- 
versity, Harris County Mosquito Control Dis- 
trict, and DVBVD show that this mosquito has 



360 



Journal of the American Mosquito Control Association Vol. 4, No. 3 




Fig. 1. Distribution of the Asian "tiger mosquito," Aedes albopietus in the United States. A-1986, B-1987. 

increased tolerance to bendiocarb, malathion, be considered by agencies using the foregoing 

and temephos, among a limited number of in- compounds. A strong source reduction program 

secticides tested to date. Rapid selection for and intensive public education can solve the 

resistance under operational conditions should albopietus problem. 



September 1988 



Spread of Ae. albopictus in the United States 



361 



Table 4. Dominance of Aedes albopictus among 
container-breeding Aedes and distance from the 
presumed focus of introduction into the United 

States. 







Ae. albopictus 




Distance from 


as percent of 


City 


Houston (mi.) 


all Aedes spp. 


Baytown 


23 


97.6 


Lafayette 


208 


40.2 


Shreveport 


214 


36.3 


Baton Rouge 


262 


33.6 


Kansas City 


662 


17.9 


Evansville 


738 


10.4 


Jacksonville 


835 


14.1 



ACKNOWLEDGMENTS 

We thank the 200 workers from 111 state and 
local health, mosquito control, university, and 
other agencies (identified in CDC 1986a, 1986b, 
1986c, 1987) for their collaboration; all those 
who helped gather these data; C. J. Bozzi, E. G. 
Campos, R. B. Craven, W. L. Jakob, B. Pafume, 
DVBVD, Fort Collins; and CDC summer survey 
team leaders L. Harrel, W. Hawley, R. Kilgen, 
A. Lowichik, J. Prullage, C. Pumpuni, and D. 
Wesson. 

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